TYPE Review

PUBLISHED 17 February 2023

DOI 10.3389/fmicb.2023.1127308

Microbial colonization and

OPEN ACCESS degradation of marine microplastics
in the plastisphere: A review
EDITED BY
JaiGopal Sharma,
Delhi Technological University,
India

REVIEWED BY Xinyi Zhai 1, Xiao-Hua Zhang 1,2,3 and Min Yu 1,2,3*

Jie Wang, 1
Frontiers Science Center for Deep Ocean Multispheres and Earth System, College of Marine Life Sciences,
China Agricultural University,
Ocean University of China, Qingdao, China, 2 Laboratory for Marine Ecology and Environmental Science,
China
Laoshan Laboratory, Qingdao, China, 3 Institute of Evolution and Marine Biodiversity, Ocean University of
Jingguang Cheng,
China, Qingdao, China
Tsinghua University,
China

*CORRESPONDENCE Marine microplastic pollution is a growing problem for ecotoxicology that needs to
Min Yu
yumin@ouc.edu.cn
be resolved. In particular, microplastics may be carriers of “dangerous hitchhikers,”
pathogenic microorganisms, i.e., Vibrio. Microplastics are colonized by bacteria,
SPECIALTY SECTION
This article was submitted to fungi, viruses, archaea, algae and protozoans, resulting in the biofilm referred to
Systems Microbiology, as the “plastisphere.” The microbial community composition of the plastisphere
a section of the journal differs significantly from those of surrounding environments. Early dominant pioneer
Frontiers in Microbiology
communities of the plastisphere belong to primary producers, including diatoms,
RECEIVED 19 December 2022
cyanobacteria, green algae and bacterial members of the Gammaproteobacteria
ACCEPTED 27 January 2023
PUBLISHED 17 February 2023 and Alphaproteobacteria. With time, the plastisphere mature, and the diversity of
CITATION
microbial communities increases quickly to include more abundant Bacteroidetes
Zhai X, Zhang X-H and Yu M (2023) Microbial and Alphaproteobacteria than natural biofilms. Factors driving the plastisphere
colonization and degradation of marine composition include environmental conditions and polymers, with the former having
microplastics in the plastisphere: A review.
Front. Microbiol. 14:1127308.
a much larger influence on the microbial community composition than polymers.
doi: 10.3389/fmicb.2023.1127308 Microorganisms of the plastisphere may play key roles in degradation of plastic in the
COPYRIGHT
oceans. Up to now, many bacterial species, especially Bacillus and Pseudomonas as
© 2023 Zhai, Zhang and Yu. This is an open- well as some polyethylene degrading biocatalysts, have been shown to be capable of
access article distributed under the terms of degrading microplastics. However, more relevant enzymes and metabolisms need to
the Creative Commons Attribution License
(CC BY). The use, distribution or reproduction
be identified. Here, we elucidate the potential roles of quorum sensing on the plastic
in other forums is permitted, provided the research for the first time. Quorum sensing may well become a new research area
original author(s) and the copyright owner(s) to understand the plastisphere and promote microplastics degradation in the ocean.
are credited and that the original publication in
this journal is cited, in accordance with
accepted academic practice. No use, KEYWORDS
distribution or reproduction is permitted which
does not comply with these terms.
microplastics, marine microorganisms, plastisphere, biodegradation, quorum sensing

1. Introduction
Plastics have the advantages of low density, good ductility, durability and low cost, and have
become widely used, worldwide. The current use of plastics is ~20 times that of half a century ago,
and it is expected that the production and use will double in the next 20 years (Urbanek et al., 2018).
Most of the plastic wastes discharged into the environment are chemically stable, corrosion-resistant,
and difficult to be degraded by microorganisms (Lambert and Wagner, 2016; Yang et al., 2020). This
has resulted in a severe environmental issue (Wright et al., 2020). It is predicted that 4.8–12.7 million
tonnes of plastics enter the oceans annually. This amount is likely to increase by an order of
magnitude within the next decade (Jambeck et al., 2015; Wright et al., 2020). Recently, the COVID-19
pandemic has driven explosive growth in the use of face masks resulting in many issues related to
their disposal (Wang et al., 2021). Indeed, it is estimated that over 129 billion face masks are used
globally each month, and over 16 million plastic particles are released from just one weathered mask
by the effect of sand (Prata et al., 2020). Plastics could be classified by physical and chemical

Frontiers in Microbiology 01 frontiersin.org

Zhai et al.
properties, such as density, molecular weight, crystallinity and
functional groups as well as the additives used, such as plasticizers,
antioxidants and flame retardants (Shah et al., 2008; Krueger et al.,
2015). The main types of “nonbiodegradable” plastics include
polyethylene (PE), polypropylene (PP), polystyrene (PS), polyethylene
terephthalate (PET) and polyvinylchloride (PVC).
Microplastics (MPs) refer to the plastic fragments of <5 mm in
diameter, and may be divided into primary and secondary MPs. Primary
MPs are directly produced and used in personal care products, such as
toothpaste and certain cosmetics, and cause direct microplastic
pollution after discarded to the environment (Zhang et al., 2018).
Secondary MPs refer to the plastic fragments that are broken up by
photodegradation, mechanical breakup, erosion and aquatic immersion
(Akdogan and Guven, 2019; Cheng et al., 2020), which are main form
of MPs present in the ocean. It is estimated that there are more than
5.25 × 1012 plastics in the surface waters of the world’s ocean, of which
the weight of MPs is ~0.35 × 105 tonnes (Eriksen et al., 2014). MPs could
be transported horizontally for long distances through the ocean
currents and wind, and vertically depending on the density of the
particles. At present, MPs have been found to be widely distributed in
the oceans, from polar regions (Peeken et al., 2018) to the equator, from
densely populated areas to remote islands (Ivar do Sul et al., 2009), and
from beaches (Claessens et al., 2011) to large ocean gyres and deep seas
(Pichel et al., 2007; Van Cauwenberghe et al., 2013). In addition, MPs
has been detected in the deepest trenches, i.e., the Mariana Trench (Peng
et al., 2018). For example, the MPs isolated from the coast of Qingdao,
China are detailed in Figure 1.
MPs have serious toxic effects on marine organisms and human
beings, as well as negative effects on the ecological environment. Firstly,
plasticizers with ecological toxic effects are released into the marine
environment. Secondly, MPs can combine with persistent organic matter
to form composite pollutants that cause enhanced toxicological effects
(Ahmad et al., 2020). Thirdly, MPs’ surface structure may be changed,
FIGURE 1
Microplastics in the coast of Qingdao, China. The black line refers to 500μm.
Frontiers in Microbiology
10.3389/fmicb.2023.1127308
and become charged in the seawater thereby increasing toxicity that may
be caused by interaction with heavy metals. The toxic substances may
be accumulated in marine animals after they ingest MPs, which lead to
damage to the biodiversity in marine environments (Ahmad et al.,
2020). Moreover, MPs may be enriched by passage through the human
body leading to adverse effects on health (Amobonye et al., 2021).
Recently, increasing concern has been raised regarding the hazard
potential of microplastic-associated microbial communities. In
particular, certain MP surfaces have been shown to exhibit selective
enrichment of bacterial pathogens—so called “dangerous hitchhikers”—
that disperse over long distances (Kirstein et al., 2016; Rummel et al.,
2017). For example, Vibrio species are enriched particularly on MPs
(Zettler et al., 2013; Frère et al., 2018; Kesy et al., 2019). The ability of
MPs to serve as carriers for dangerous hitchhikers poses threats to both
aquatic ecosystems and human health. Besides colonization with
pathogens, MPs could act as a long-term reservoir for antibiotic
resistance (Liu et al., 2021).
The damage of MPs to biodiversity and ecosystem health is
increasing in significance, especially with regards to microorganisms.
Elucidating the role of MPs in the microbial loop and the role of
microorganisms in the degradation of MPs is of great value (Amaral-
Zettler et al., 2020). This may provide insights for the design of efficient
degradation enzymes, and thereby reduce damage to human beings and
the environment. This article reviews the current knowledge of the
bacterial composition of the MP biofilms, the biodegradation of MP, and
the relationship between plastisphere and quorum sensing (QS).
2. Formation of the plastisphere
MPs can provide advantages to the colonizing microbial
communities, including physical support, nutrient supply and habitats
that help microorganisms to resist harsh environmental conditions
02 frontiersin.org
Zhai et al.
(Oberbeckmann and Labrenz, 2015; Shen et al., 2019; Ahmad et al.,
2020). As with any kind of surface, microorganisms attach to and
colonize MP surfaces immediately after the material enter the aquatic
ecosystem, forming MP biofilms that have been termed the
“plastisphere” (Zettler et al., 2013). The plastisphere may be regarded as
a new micro-ecosystem in pelagic waters, and include primary
producers, predators, symbionts, and decomposers (Amaral-Zettler
et al., 2020). The microbial communities in the plastisphere are
composed of a diverse range of bacteria, fungi, viruses, archaea, algae,
and protozoans (Wright et al., 2020).
2.1. Formation and succession
The growth of the microbial community on MP biofilms represents
a temporal succession process that may be divided into different stages
(Yang et al., 2020). In the initial colonization stage, the pioneer
microorganisms are able to form microbial assemblages, and cover the
maximum possible surface area of plastic. These generalist organisms
proliferate without competition other than to grow faster than the rest
to cover the surface (Wright et al., 2020), and pave the way for the
enhanced attachment of other microorganisms, and recycling of
resources (Onda and Sharief, 2021). As the biofilm grows, within days
microorganisms attach to the plastic surface irreversibly, followed by a
succession of other bacteria, viruses and eukaryotic microorganisms
(Onda and Sharief, 2021). This is achieved by pili, adhesion of proteins,
and production of complex extracellular polymeric substances (EPS),
which facilitate adhesion to surfaces and stablish cell–cell interactions
(Dussud et al., 2018). The secondary metabolites may improve quorum
sensing and the antimicrobial effect to resist competing microorganisms
(Davey and O’Toole, 2003; Hall-Stoodley et al., 2004; Carozza et al.,
2015). Processes involve catalyzing metabolic reactions, including
adsorption, desorption, and fragmentation of microplastic-associated
compounds (Harrison et al., 2011; Urbanek et al., 2018). Finally, the
continuous recruitment, loss, and replacement of species transform the
structure into a hotspot for diverse interacting communities (Onda and
Sharief, 2021), resulting in a mature plastisphere. For example,
maturation phase of the PE plastisphere appeared after 30 days
immerging in seawater, and a stabilization of bacterial abundance and
heterotrophic bacterial production without significant increase was
reached (Cheng et al., 2020). However, there was a drastic shift in
bacterial community structure in maturation phase (Cheng et al., 2020).
The formation of and succession in the plastisphere is described in
Figure 2.
Early dominant pioneer communities in marine and estuarine
plastispheres belong to primary producers including diatoms,
cyanobacteria, green algae (Zettler et al., 2013; Bryant et al., 2016) and
bacterial members of Gammaproteobacteria and Alphaproteobacteria
(Lee et al., 2008; Oberbeckmann and Labrenz, 2015). As for
Gammaproteobacteria, Oceanospirillaceae and Alteromonadaceae
representatives were present, and which could occur up to 59.1% of the
total microbial community after 1 day of immersion of the MPs in the
marine habitat. Their presence decreased significantly later (Pollet et al.,
2018; Roager and Sonnenschein, 2019). Also, Vibrio spp. were early
colonizers of PE and PS in marine environments (Kesy et al., 2019).
Alcanivorax, Aestuariicella, and Marinobacter were the dominant early
colonizers on different plastic substrates (Dussud et al., 2018). In
addition, the families Saprospiraceae and Oscillatoriaceae were found on
early stages of the plastisphere (Oberbeckmann et al., 2016). With the
Frontiers in Microbiology
10.3389/fmicb.2023.1127308
plastisphere becoming mature, the abundance of distinct microbial
communities, including Bacteroidetes (Lee et al., 2008) and
Alphaproteobacteria (Pollet et al., 2018), increased quickly on the
plastisphere. For example, Bacteroidetes were always significantly more
abundant at later stages (Hadad et al., 2005). In contrast,
Rhodobacteraceae came early to MPs, and they were persistent and
became dominant as time passed (Pollet et al., 2018). Rhodospirillaceae,
including purple sulfur bacteria, may fix N2 and thus provide “fertilizer”
to other community members. In addition, flavobacteria,
Planctomycetaceae and Phyllobacteriaceae were abundant at the later
stages of the MPs colonization (Pinto et al., 2019).
2.2. Microbial community composition
The microbial community composition of the plastisphere
represents the main research target, and many studies revealed
significant differences from microhabitats in the same environment
(Bryant et al., 2016; Oberbeckmann et al., 2018; Ogonowski et al., 2018).
Proteobacteria, Bacteroidetes, Firmicutes and Cyanobacteria are usually
the main bacteria enriched in the plastisphere. This differs from a range
of other substrates, such as metal, rubber, glass, fabric, and seawater
(Ogonowski et al., 2018; Woodall et al., 2018). Moreover, there was a
different abundance and distribution pattern of photosynthetic and
heterotrophic bacteria in plastic samples compared with those in
seawater (Zettler et al., 2013). These data indicate that the plastisphere
is a specific ecological niche where microorganisms with potential
metabolic adaptations, specific metabolic pathways (including
attachment, chemotaxis, additive resistance, degradation, secretion,
nitrogen fixation and motility) were enriched (Roager and
Sonnenschein, 2019). Studies on microbial community composition of
the plastisphere based on research methods of field sampling and in situ
incubation are summarized in Table 1.
2.2.1. Diatoms
Diatoms (phototrophic organisms) are common residents of the
plastisphere, and are often reported as early and even dominant
colonizers on plastic debris (notably the plastics exposed to sunlight;
Table 1). For example, diatoms dominated in the microbial community
on the abundant MPs in the Eastern North Pacific Gyre (Carson et al.,
2013). Although the dominate role of diatoms declines with plastisphere
maturing, they remain consistent members in the plastisphere (Amaral-
Zettler et al., 2020).
2.2.2. Cyanobacteria
As another photosynthetic organism, Cyanobacteria join with
diatoms to typically contribute net primary production on MPs,
providing nutrients for heterotrophs in the plastisphere. Many studies
have shown that Cyanobacteria are dominate candidates of the
plastisphere, especially in the early stages (Table 1). For example, the
genera Stanieria and Pseudomorphium were found abundant on PET
across stations (Orr et al., 2004). In particular, the genus Phormidium
was found commonly in microbial mat on various substrates, and has
been found to be present on PE, PET, and PP samples (Table 1). This
genus was identified as an important member of a plastic-colonizing
community in the North Atlantic (Zettler et al., 2013), and also
determined to degrade hydrocarbons (Antić et al., 2006). In addition,
filamentous cyanobacteria, Phormidium, occurred on plastics, but was
absent from seawater samples (Zettler et al., 2013). Sunlight exposure
03 frontiersin.org
Zhai et al.
FIGURE 2
The formation of and succession in the plastisphere.
on floating MPs may well be beneficial to the enrichment of this
photosynthetic organism on plastic debris.
2.2.3. Proteobacteria
As the most abundant phylum globally, Proteobacteria comprise the
most enriched phylum on the plastisphere in comparison with
populations in seawater. As is shown in Table 1, within the phylum
Proteobacteria, the classes Alphaproteobacteria, Gammaproteobacteria,
Betaproteobacteria, and Deltaproteobacteria are enriched on
plastic samples.
Many studies showed that the family Rhodobacteraceae, within
class Alphaproteobacteria, occupied the core population of the
plastisphere (Table 1). Rhodobacteraceae, especially Roseobacter,
was recognized as a primary colonizer of various substrates in
marine environments (Dang et al., 2008). However, these organisms
were found to be enriched significantly on marine plastic debris as
compared with organic particles (Dussud et al., 2018) and seawater
(Erni-Cassola et al., 2020). In fact, Rhodobacteraceae is not only the
primary colonizer, but is also abundant at all colonization periods,
and exerts an important role in biofilm formation. This reflects the
extracellular polymeric substance (EPS) produced by
Rhodobacteraceae after colonizing new surfaces, leading to
enhancing the settlement of other microorganisms (Amaral-Zettler
et al., 2020). Apart from Rhodobacteraceae, bacteria belonging to
the family Erythrobacteraceae have been found on various macro−/
micro-plastics (Table 1). Moreover, hydrocarbonoclastic bacteria
were overrepresented in the plastic fraction (Dussud et al., 2018).
Within Gammaproteobacteria, the order Pseudomonadales has been
highlighted (Oberbeckmann et al., 2018; Sun et al., 2020; Zhang et al.,
2021b). Pseudomonas was found to have biodegradation potential on
MPs (as discussed later) leading to interest for MP-degradation research.
As is shown in Table 1, Vibrio is another member of the
Gammaproteobacteria detected widely on MPs in marine environments
(Zettler et al., 2013; Sun et al., 2020; Xie et al., 2021). Many Vibrio spp.
are pathogenic and regarded as dangerous hitchhikers on MPs facilitating
their spread widely throughout the marine environment. Vibrio spp. are
usually primary colonizers, and grow rapidly with the ability to dominate
on the plastisphere in comparison with natural seston (Frère et al., 2018;
Kesy et al., 2019). Moreover, the order Oceanospirillales and the family
Alcanivoraceae have been found in the plastisphere (Oberbeckmann
et al., 2016; Syranidou et al., 2019; Table 1).
Frontiers in Microbiology
10.3389/fmicb.2023.1127308
2.2.4. Bacteriodetes
Bacteriodetes is the second most represented bacterial phylum on
plastic surfaces (Table 1). Here, the distribution of Bacteroidetes do not
reveal clear temporal patterns, and is dominated constantly by
Flavobacteria. These may well be essential members, and key players in
the formation of biofilms (Pollet et al., 2018). The class Flavobacteria has
been recognized as colonizers on various MPs, including PS, PE, PP, and
PET (Table 1). For example, the family Flavobacteriaceae occurred more
frequently on PET particles compared with glass beads (Oberbeckmann
et al., 2016), and PE and PS compared with wooden pellets
(Oberbeckmann et al., 2018). Flavobacteriaceae has been described as a
keystone taxon in biofilms that feed off exudates from dinoflagellates
and diatoms (Amin et al., 2012).
The order Sphingobacteriales and genus Lewinella have been
reported frequently as colonizers of the plastisphere (Zettler et al., 2013;
Oberbeckmann et al., 2016; Debroas et al., 2017; Jiang et al., 2018;
Ogonowski et al., 2018). Sphingobacteriales was shown capable of
metabolizing polycyclic aromatic hydrocarbons (PAHs; Leys et al., 2004)
and abundant in both short-term (60 days) and long-term (5 months)
MP samples after outside incubation in North Seawater (Kirstein
et al., 2019).
2.2.5. Firmicutes
Firmicutes was found among the most abundant populations
enriched on marine PS samples (Syranidou et al., 2019). In particular,
the genus Bacillus has revealed a wide-spread and powerful
biodegradation potential on various kinds of MPs, namely PE, PP, PS,
PVC, and PET.
2.3. Factors influencing the formation of the
plastisphere
Factors driving the microbial composition in the plastisphere are
complex, and may be divided into environmental and polymer
characteristic factors. Environmental aspects include physicochemical
factors (namely temperature, salinity, depth, pH, dissolved oxygen and
light), nutrient availability (e.g., organic/inorganic carbon, ammonium,
nitrate, nitrite and phosphorus) for microbial growth, pollutants (e.g.,
toxic metals, antibiotics and persistent organic pollutants), and biotic
factors (principally algae and animals; Yang et al., 2020). Also, polymer
04 frontiersin.org
Zhai et al. 10.3389/fmicb.2023.1127308

TABLE 1 Studies on the plastisphere based on sampling site and time, plastic type and microbial community.

Sampling site Month Plastic types Core communities Research References

method
Western 4–11 PE PP PS Cyanobacteria (40.8%, mainly Pleurocapsa sp. Field sampling Dussud et al. (2018)
Mediterranean Sea Oscillatoriales, Chroococcales, Nostocales and
Pleurocapsales orders, Synechococcus sp., Calothrix sp.,
Scytonema sp. and Pleurocapsa sp.)
Alphaproteobacteria (32.2%, mainly Roseobacter sp.)

The North Atlantic 10, 12 PE PP PS Alphaproteobacteria (17.67% ± 5.28%) Field sampling Frère et al. (2018)
Gammaproteobacteria (40.76% ± 8.43%) Flavobacteria
(16.83% ± 2.64%) Cyanobacteria (9.09% ± 7.40%)

The North Atlantic 6 PE PET PS Alphaproteobacteria, Streptomycetales, Bacteroidetes Field sampling Debroas et al. (2017)
and Cyanobacteria

North Sea 3, 6, 9 PE PP Alphaproteobacteria, Gammaproteobacteria and Field sampling De Tender et al. (2015)
Bacteroidetes

North Sea 9–7 PE Proteobacteria and Bacteroidetes In situ incubation De Tender et al. (2017)

Mediterranean Sea 11 PE PP Bacteroidetes, Gammaproteobacteria and Field sampling Delacuvellerie et al.

Alphaproteobacteria (2019)

The Yangtze estuary 4 PE PP PS Proteobacteria, Cyanobacteria, Bacteroidetes and Field sampling Jiang et al. (2018)
Actinobacteria

The North Atlantic 5, 6, 7 PP PE Vibrio sp. Field sampling Zettler et al. (2013)

The equatorial 10–12 PVC PE PA Proteobacteria (52%), Bacteroidetes (10%), and Field sampling Woodall et al. (2018)
Atlantic Crenarchaeota

The Eastern North 7 PE PP PS Bacillus bacteria and pennate diatoms Field sampling Carson et al. (2013)
Pacific

North Sea 1, 7 PE PP Bacteriodetes, Cyanobacteria and Proteobacteria Field sampling Oberbeckmann et al. (2014)

Baltic Sea 8, 9 HDPE PS Flavobacteriaceae, Rhodobacteraceae and In situ incubation Oberbeckmann et al.
Planctomycetaceae (2018)

The North Pacific 8 PE PP Cyanobacteria and Alphaproteobacteria Field sampling Bryant et al. (2016)

Baltic Sea 8 PE PP PS Alphaproteobacteria and Sphingomonadaceae In situ incubation Ogonowski et al. (2018)

Mediterranean Sea – PVC Gammaproteobacteria (Oceanospirillaceae and In situ incubation Pollet et al. (2018)
Alteromonadaceae), Alphaproteobacteria
(Rhodobacteraceae) and Bacteroidetes (Flavobacteriia)

Mediterranean Sea – PS Proteobacteria and Firmicutes Field sampling Syranidou et al. (2019)

South China Sea 5, 8 PS Rhodobacteraceae and Sphingomonadaceae In situ incubation Lee et al. (2014)

South China Sea, 4, 7, 11, 1 PP PVC Alphaproteobacteria (Rhodobacteraceae) and Field sampling Xu et al. (2019)
the Yellow Sea Gammaproteobacteria

Mediterranean Sea 8 PE Roseobacter, Oleiphilus, and Aestuariibacter In situ incubation Erni-Cassola et al. (2020)

Baltic Sea 2 PE PP PS Gammaproteobacteria (47%–81%), In situ incubation Hansen et al. (2021)

Alphaproteobacteria (7%–34%) and Bacteroidia (3%–
20%)

Mediterranean Sea 10 PE Gammaproteobacteria, Alphaproteobacteria and Field sampling Sucato et al. (2021)
Bacteroidetes

The Yellow Sea 8 – Vibrio, Pseudoalteromonas and Alteromonas In situ incubation Sun et al. (2020)

North Sea – PE PP PS PVC Alphaproteobacteria (18%–53%) and In situ incubation Kirstein et al. (2019)
PET Gammaproteobacteria (20%–75%)

Southern Ocean 2 (summer in HDPE Gammaproteobacteria and Betaproteobacteria Field sampling Cappello et al. (2021)
Southern Hemisphere)

Mangrove in China 4, 7 PP PS Vibrio, Rhodobacteraceae, Alteromonadaceae and In situ incubation Xie et al. (2021)
Pseudoalteromonadaceae

Bohai Sea 7, 8, 9 PVC PP PE PS PU Gammaproteobacteria (Vibrio, Pseudoalteromonas) In situ incubation Zhang et al. (2021b)
and Bacteroidetes
PE, polyethylene; PP, polypropylene; PS, polystyrene; PET, polyethylene terephthalate; PVC, polyvinylchloride; PU, polyurethane; HDPE, high density polyethylene.

Frontiers in Microbiology 05 frontiersin.org

Zhai et al.
characteristic factors include the type, surface property and size of
the plastics.
Environmental factors related to geography have a larger influence
on the plastisphere community than the plastic type (Oberbeckmann
et al., 2018; Kesy et al., 2019). Studies on microbial communities on
different polymer types floating in the North Pacific and North Atlantic
demonstrated that plastisphere communities were well-defined
biogeographically, displaying latitudinal gradients in species richness,
and to a lesser extent between polymer types (Amaral-Zettler et al.,
2016). As is shown in Table 1, core microbial communities in marine
environments show clear geographical distribution patterns, which may
influence the formation of specific plastispheres. So far, studies
investigating the plastisphere in various marine environments are
mainly focused in Europe (Mediterranean Sea, North Sea and Baltic
Sea) and China, and to a lesser extent the Atlantic, Pacific and Southern
Ocean (Table 1).
Apart from geography, there are other environmental factors
influencing the plastisphere community. Microbial diversity and
function show strong dependency on environmental conditions, in
turn influencing MP biofilm formation and structure (Yang et al.,
2020). And the early attachment and succession of plastisphere are
affected by the growth rate of the biofilm, determined by factors
including temperature, light, and nutrient availability (Wright et al.,
2020). For instance, the light availability was shown to play a key role
in shaping plastisphere communities, and revealed that environmental
variables, not plastic type, had the largest impact on microbial
composition (Wright et al., 2021). In addition, microbial communities
in the plastisphere along an environmental gradient were shaped
more by salinity than by plastic type (Oberbeckmann et al., 2018;
Jacquin et al., 2019). Indeed, salinity gradients influenced microbial
communities in the plastisphere significantly (Oberbeckmann et al.,
2018), particularly enhancing the abundance of Gammaproteobacteria
(Oberbeckmann et al., 2018; Kesy et al., 2019). Moreover, ocean
acidification altered bacterial communities on marine plastic debris
(Harvey et al., 2020). It was noteworthy that the light intensity was
negatively correlated with depth, which could cause the depth-
dependent distribution of photosynthetic bacteria. Photoautotrophic
bacteria, such as cyanobacteria, i.e., the genera Phormidium and
Rivularia, dominated the plastisphere communities living in surface
seawater, whereas the core microbiome of the plastisphere living on
the seafloor and sub-surface seawater appeared to comprise
Bacteroidetes (Flavobacteriaceae) and Proteobacteria
(Rhodobacteraceae and Alcanivoracaceae; Jacquin et al., 2019).
In addition, the abundance of the microbial community of the
plastisphere is influenced by the size and especially the type of plastic
(Frère et al., 2018; Wright et al., 2021). This may be attributed to the
chemotactic selectivity colonization on MPs with different polymer
chemical properties (Xie et al., 2021). The results in a situ exposure
experiments for nine different types of MPs, including low density
polyethylene (LDPE), PS, expanded polystyrene (EPS), PP,
polycarbonate (PC), polyamide 6 (PA6), PVC, PET, and acrylonitrile
butadiene styrene (ABS) in mangrove, revealed that MPs with different
chemical structures would attract different microbial colonizers (Xie
et al., 2021). Hansen et al. (2021) quantified the biofilm on PE, PP, and
PS by six marine bacterial strains (Vibrio, Pseudoalteromonas and
Phaeobacter), demonstrating that each one had a unique colonization
behavior with either a preference for PS or PP over the other polymer
types, or no preference at all. Wright et al. (2021) re-analyzed all
plastisphere studies that utilize 16S rRNA gene amplicon sequencing,
Frontiers in Microbiology
10.3389/fmicb.2023.1127308
and found that Oceanospirillales and Alteromonadales were more
abundant in plastic samples than control biofilms, with Oceanospirillales
generally being more abundant in aliphatic plastic samples, and
Alteromonadales in other plastics. In addition, the roughness,
hydrophobicity and age of MPs could clearly influence microbial
community structure of plastisphere (Yang et al., 2020). Interestingly,
differences in microbial composition between polymers are usually
caused by rare taxa whereas the abundant microbial groups remain
largely unchanged (Ivk et al., 2018).
Plastisphere development does rely largely on the surrounding
microbial communities although there are significant differences
between them (Arias-Andres et al., 2018). In fact, consistent conclusions
have not been made when studying the microbial community
compositions of the plastisphere in marine environments because of the
variety of plastic substrate types, season and geographical location
(Oberbeckmann et al., 2014). For example, early attachment and
succession of the plastisphere depend on the growth rate of the biofilm,
determined by physicochemical factors and nutrient availability. There
may well be some polymer-specific communities in the initial
colonization, which are largely influenced by the differences between
materials, such as additives or preweathering, and will eventually
converge over time (Amaral-Zettler et al., 2020).
2.4. Ecological effects of the plastisphere
The plastisphere has multiple effects on the fate of plastics and the
marine environment (Cheng et al., 2020). Firstly, the plastisphere may
change the density of MP particles, making them susceptible to
vertical transport by sinking and floating (Lagarde et al., 2016).
Secondly, the plastisphere may change the adsorption state of the MP
surface, and affect the decomposition rate of the MPs in seawater. In
the biofilm, autotrophic microorganisms may accelerate the oxidative
decomposition of MPs by producing oxygen during photosynthesis.
Heterotrophic microorganisms may degrade MPs by a series of
processes, including biodeterioration, bio-fragmentation,
bio-assimilation and biomineralization. Conversely, the plastisphere
may slow down the photochemical decomposition process of MPs by
ultraviolet light (Onda and Sharief, 2021). Moreover, microorganisms
colonizing MPs may be transported vertically and for long-distances
horizontally in the ocean, which may promote the diffusion of invasive
species to fragile ecosystems (Gregory, 2009). Pathogens, such as
Vibrio, Tenacibaculum, Pirellulaceae (Wright et al., 2021) and
spirochetes (Xie et al., 2021), were usually found on MPs. When algal
blooms and infectious diseases caused by pathogens occur, the
negative influence on marine ecosystems is significant (Zettler et al.,
2013; Rummel et al., 2017). Therefore, the risk of MPs carrying
pathogens to infect humans and cause long-distance transmission
should be determined (Xie et al., 2021).
3. Biodegradation of microplastic
The biodegradation of plastics may be defined as the process that
microorganisms digest and decompose plastic fragments into available
carbon sources by changing the plastics functional group structure,
molecular weight, tensile property and other features associated with the
polymers. The microbial degradation of MPs is affected by
microorganisms, MPs properties, and environmental factors.
06 frontiersin.org
Zhai et al.
3.1. Microorganisms involved in
microplastic/plastic degradation
Up to now, information regarding the microorganisms involved in
plastic degradation is rudimentary. Currently, the microorganisms
capable of degrading MPs are mainly associated with the terrestrial
environment, and more so for PE degradation, and include
Achromobacter, Acinetobacter, Arthrobacter, Aspergillus (fungus),
Bacillus, Comamonas, Delftia, Micrococcus, Nesiotobacter, Paenibacillus,
Pseudomonas, Rahnella, Staphylococcus, and Stenotrophomonas. These
have been isolated from various soil environments, saltpan water and
landfills (Table 2). Bacteria capable of degrading PET include Ideonella
and Saccharomonospora, which were isolated from a PET bottle
recycling site and recovered from compost, respectively (Kawai et al.,
2014). Pseudomonas, Bacillus and Achromobacter were demonstrated to
degrade PVC (Das et al., 2012; Giacomucci et al., 2019). Aspergillus
showed the ability to degrade PU (Khan et al., 2017). Moreover,
Thermus, Bacillus and Geobacillus, which were isolated from a sludge
composting pool, degraded PS, suggesting that hyperthermophilic
composting was a promising strategy for MPs removal from organic
wastes (Chen et al., 2020). Bacillus and Pseudomonas, capable of
degrading high impact polystyrene (HIPS), were obtained from landfills
(Mohan et al., 2016). Aspergillus, Bacillus, Pseudomonas, Staphylococcus,
and Streptococcus were isolated from different soil samples, and were
capable of degrading PET and PS (Asmita et al., 2015). In addition, a
Rhodococcus strain isolated from soil burying PE mulch was capable of
degrading both PS and PE (Orr et al., 2004; Mor and Sivan, 2008).
It is noteworthy that Bacillus and Enterobacter in waxworm gut
could “eat” PE (Yang et al., 2014), whereas Exiguobacterium (Yang et al.,
2015a,b), Bacillus anthracis, Enterobacter hormaechei, and Aspergillus
niger (Kong et al., 2018) in mealworm gut could attack PS. In addition,
the marine polychaete Marphysa sanguinea inhabiting PS debris was
able to degrade PS particles (Jang et al., 2018). Certainly, studying the
microfauna and gut microorganisms may be an innovative way for the
treatment of plastic waste.
At present, studies on the microbial degradation of marine plastics
are limited, and mainly involve the enrichment and isolation of plastic
degrading microorganisms in the offshore environment. Thus,
Arthrobacter, Aspergillus, Bacillus, Kocuria, Pseudomonas and Zalerion
maritimum (fungus) demonstrated the capability of degrading PE, and
Bacillus could degrade PVC (Table 2). Pseudomonas, isolated from
plastics immersed for several days in Bay of Bengal, was found have a
great ability to degrade PP, LDPE and HDPE (Sudhakar et al., 2007).
Furthermore, Pseudomonas aeruginosa E7, which was isolated from
beach soil contaminated by an oil spill, displayed high degradative
activity to low-molecular-weight polyethylene (LMWPE), and
metabolized 40.8% of the carbons of LMWPE into CO2 after 80 days of
composting (Jeon and Kim, 2015). Pseudomonas and Lysinibacillus,
which were isolated from deep-sea sediment, used an increased
extracellular matrix to improve cell adhesion to weathered HDPE
(Oliveira et al., 2021). Other examples include Rhodococcus and Bacillus,
which were isolated from mangrove, and were capable of degrading
several kinds of MPs (Auta et al., 2017, 2018). Moreover, after 40 days of
incubation, weight losses of PE, PET, PP, and PS particles were found
and it was resulted from the action of Bacillus cereus and Bacillus
gottheilii (Auta et al., 2017). Bacillus sp. strain 27 and Rhodococcus sp.
strain 36 could also degrade PP and cause weight losses (Auta et al.,
2018). Apart from aerobic bacteria, anaerobic marine consortia were
found degrade PVC (Giacomucci et al., 2020).
Frontiers in Microbiology
10.3389/fmicb.2023.1127308
As is shown in Table 2, Bacillus and Pseudomonas were very important
bacteria in the degradation of MPs. Among the 15 strains of bacteria
capable of degrading HDPE isolated from the coast, Pseudomonas was the
most efficacious (Balasubramanian et al., 2010). Pseudomonas spp.
achieved a percentage weight reduction of PE of up to 20% within 120 days
(Kyaw et al., 2012). The metabolites of PS decomposed by Pseudomonas
were styrene, toluene and benzene, which could be easily used by other
bacteria (Shah et al., 2008). A novel carboxylic ester hydrolase was
identified in the genome of the marine bacterium Pseudomonas aestusnigri,
indicating its significant potential for PET degradation (Bollinger et al.,
2020). It seems that the degradation ability of Pseudomonas is partly due to
the high hydrophobicity of the cell surface, which is conducive to its
adhesion to the polymer, and the formation of biofilm to promote
degradation. In addition, the secretion of extracellular polysaccharide is
important to promote the degradation of LDPE. However, the degradation
effects vary with types of plastics (Shah et al., 2008).
Biofilm has an important effect on biodegradation, which relies on
the influence of nutritional conditions for its formation. An alteration
of Pseudomonas surface hydrophobicity was detected by the change of
glucose and ammonium sulfate concentrations (Tribedi and Sil, 2014).
Thus, the increased cell surface hydrophobicity promoted the efficient
formation of biofilm in a polyethylene succinate film, which was
positively correlated to degradation (Tribedi and Sil, 2014). Conversely,
in the presence of marine sediments, which were organic carbon-rich,
biofilm formation was diminished, and the degradation of PE was
minimal (Nauendorf et al., 2016). Therefore, environmental and
nutritional conditions that favor the genesis of biofilms on plastic
polymers are important stimuli for the degradation of synthetic plastics
by Pseudomonas (Wilkes and Aristilde, 2017).
A toxic metabolite produced by one microorganism may be a
substrate for the growth of another, thus eliminating the toxic effects to
the former (Yuan et al., 2020). Conversely, symbiotic interactions in
consortia increased the activity and tolerance for the treatment of
pollutants (Singh and Wahid, 2015; Yuan et al., 2020). For example,
Bacillus and Paenibacillus reduced the dry weight of MP particles (14.7%
after 60 d) and the mean particle diameter (22.8% after 60 d) when in a
bacterial consortium (Park and Kim, 2019). Moreover, a marine
bacterial community composed of Idiomarina, Marinobacter,
Exiguobacterium, Halomonas, and Ochrobactrum was capable of
colonizing and degrading PET and PE efficiently (Gao and Sun, 2021).
3.2. Mechanism and enzymes of microplastic
biodegradation
The mechanisms and enzymes of MP biodegradation have not been
fully elucidated. Overall, the process of microbial degradation of MPs
may be divided into colonization, depolymerization, assimilation and
mineralization (Pathak, 2017), which involve multiple biochemical
reactions. After colonization on the surface of MPs, microorganisms
release extracellular enzymes to combine with polymers and cleave
them. This leads to depolymerization into low molecular weight
oligomers, dimers and even monomers (Shah et al., 2008). The processes
involve hydrolysis (for hydrolyzable plastics) and oxidative degradation
(for hydrolyzable and non hydrolyzable plastics). After depolymerization,
the oligomers enter the cells, and serve as the carbon source for
microbial growth, which is assimilation. The mineralization refers to the
decomposition of different types of MPs into small molecules, such as
CO2, CH4 and H2O, through the TCA cycle (Figure 3). Up to now, the
07 frontiersin.org
Zhai et al. 10.3389/fmicb.2023.1127308

TABLE 2 Bacteria capable of degrading MPs.

Plastic types Microorganism Environment Sampling site Research Reference

progress
LDPE Bacillus mycoides Acinetobacter Land Waste coal soil in Poland Isolation and culture Nowak et al. (2011)
baumannii Pseudomonas fluorescens
Staphylococcus cohnii Staphylococcus
xylosus

LDPE Bacillus cereus Micrococcus luteus Land Forest soil in Poland Isolation and culture Nowak et al. (2011)
Micrococcus lylae Rahnella aquatilis
Arthrobacter viscosus

LDPE Bacillus pumilus Paenibacillus macerans Land Crater soil in Poland Isolation and culture Nowak et al. (2011)
Bacillus thuringiensis Bacillus
amyloliquefaciens Micrococcus luteus

LDPE Bacillus Paenibacillus Land Landfill site in Korea Isolation and culture Park and Kim (2019)

LDPE Aspergillus clavatus* Land Landfill soil in India Isolation and culture Gajendiran et al. (2016)

LDPE Rhodococcus ruber Land Soil burying PE mulch in Isolation and culture Oberbeckmann et al.
Israel (2014)

LDPE Nesiotobacter exalbescens Bacillus Land Saltpan water in India Isolation and culture Deepika and Madhuri
vietnamensis (2015)

LDPE Pseudomonas Land Waste dumping ground Hydrolase Tribedi and Sil (2014)
soil in India

LDPE Bacillus Enterobacter asburiae Worm gut Waxworm gut Isolation and culture Yang et al. (2014)

LDPE Pseudomonas aeruginosa Marine Soil from an oil-spill Alkane monooxygenase, Jeon and Kim (2015)
beach in Korea rubredoxin, rubredoxin
reductase

LDPE Kocuria palustris Bacillus pumilus Bacillus Marine Sea water of the Arabian Isolation and culture Harshvardhan and Jha
subtilis Sea coast in India (2013)

LDPE HDPE Bacillus sphericus Bacillus cereus Marine Shallow waters of the Isolation and culture Sudhakar et al. (2007)
Indian Ocean

HDPE Delftia Comamonas Stenotrophomonas Land Plastic debris from Isolation and culture Peixoto et al. (2017)
Cerrado Soil in Brazil

HDPE Achromobacter xylosoxidans Land Polyethylene bags and soil Isolation and culture Kowalczyk et al. (2016)
of waste sites in Poland

HDPE Arthrobacter Pseudomonas Marine Soil of coastal plastic Isolation and culture Balasubramanian et al.
waste Dumped sites in (2010)
India

HDPE Aspergillus tubingensis* Aspergillus Marine Plastic waste dumped Isolation and culture Sangeetha Devi et al.
flavus* Marine environmental site (2015)
in India

HDPE Pseudomonas Lysinibacillus Marine Deep-sea sediment from Isolation and culture Oliveira et al. (2021)
Pelotas Basin in Brazil

PE Zalerion maritimum* Marine Strain culture Laccase Paço et al. (2017)

PE PVC Bacillus Marine Sea water of Gujarat coast Isolation and culture Kumari et al. (2019)
in India

PE PET Exiguobacterium, Halomonas, Marine Coast of Qingao, China Esterase and hydrolase Gao and Sun (2021)
Ochrobactrum sp

PET Alcanivorax Hyphomonas Cycloclasticus Marine Messina Strait Isolation and culture Denaro et al. (2020)

PET Stanieria Pseudomorphium Marine The North Sea off the KEGG Orr et al. (2004)
United Kingdom coast

PET Ideonella sakaiensis Land Sediment from PET bottle PETase MHETase Yoshida et al. (2016)
recycling site in Japan

PET Saccharomonospora viridis Land Compost in Japan Cutinase Kawai et al. (2014)

(Continued)

Frontiers in Microbiology 08 frontiersin.org

Zhai et al. 10.3389/fmicb.2023.1127308

TABLE 2 (Continued)

Plastic types Microorganism Environment Sampling site Research Reference

progress
PET PS Pseudomonas aeruginosa Bacillus subtilis Land Five different soil samples Isolation and culture Asmita et al. (2015)
Staphylococcus aureus Streptococcus in India
pyogenes Aspergillus niger*

PS Rhodococcus ruber Land Soil burying PE mulch in Isolation and culture Mor and Sivan (2008)
Israel

PS Thermus Bacillus Geobacillus Land Sludge composting plant Isolation and culture Chen et al. (2020)
in China

PS Bacillus anthracis Enterobacter Worm gut Mealworm gut Isolation and culture Kong et al. (2018)
hormaechei Aspergillus niger*

PS Exiguobacterium Worm gut Mealworm gut Isolation and culture Yang et al. (2015a,b)

PS PE PET PP Bacillus.cereus Bacillus.gottheilii Mangrove Mangrove sediment in Isolation and culture Auta et al. (2017)
Malaysia

HIPS Bacillus Pseudomonas Land Plastic dump yard soil in Esterase Mohan et al. (2016)
India

PP Bacillus Rhodococcus Mangrove Mangrove sediment in Isolation and culture Auta et al. (2018)
Malaysia

PVC Pseudomonas citronellolis Bacillus flexus Land Strain culture Pure culture Giacomucci et al. (2019)

PVC Pseudomonas aeruginosa Achromobacter Land Crude oil contaminated Isolation and culture Das et al. (2012)
soil in India

VC Ochrobactrum Pseudomonas putida Land Waste site groundwater in Alkene monooxygenase Danko et al. (2004)
America

PU Aspergillus tubingensis* Land Dumping area in Pakistan Isolation and culture Khan et al. (2017)

*Fungus.
PE, polyethylene; HDPE, high density polyethylene; LDPE, low density polyethylene; PP, polypropylene; PS, polystyrene; PET, polyethylene terephthalate; PVC, polyvinylchloride; PU, polyurethane;
VC, vinyl chloride.

plastic degrading enzymes have been reported to include hydrolases
(such as esterase, lipase, keratinase, and cutinase) and oxidoreductases
(such as laccase, manganese peroxidase, hydroxylase and lignin
peroxidases) (Gan and Zhang, 2019; Zhang et al., 2021a).
PE degrading biocatalysts include hydroxylase, laccase, peroxidase
and reductase (Amobonye et al., 2021). A manganese peroxidase was
identified in two types of fungi leading to degradation of PE (Iiyoshi et al.,
1998). Laccase, which is produced by Actinomycetes, Rhodococcus,
Aspergillus flavus and Pleurotus ostreatus, degraded PE significantly (Santo
et al., 2013; Gómez-Méndez et al., 2018; Zhang et al., 2020). With
Pseudomonas aeruginosa, alkane hydroxylase was involved directly in the
biodegradation of LMWPE. Also, rubredoxin and rubredoxin reductase
exerted an indirect role through the transfer of related electrons (Jeon and
Kim, 2015). In addition, alkane hydroxylase, which was produced by
Pseudomonas sp. E4, played an important role in the degradation of PE
through the oxidation of the PE main chain (Yoon et al., 2012).
Although the microbial degradation of PS by various bacteria and
fungi has been demonstrated, the major enzymes involved in the initial
depolymerization have not been clearly identified (Amobonye et al.,
2021). An extracellular esterase from Lentinus tigrinus (Tahir et al.,
2013) and certain polymerases from Bacillus and Pseudomonas (Mohan
et al., 2016) have been shown to degrade PS. It was determined that
styrene monooxygenases (SMO), styrene oxide isomerase (SOI),
phenylacetaldehyde dehydrogenase (PAD) and multiple enzymes of
phenylacetate degradation (PAA#) could degrade PS into styrene oxide,
phenylacetaldehyde, phenylacetate and phenylacetic acid (an
intermediate product of TCA cycle; Tischler et al., 2009).
Many hydrolases, including lipase, esterase and keratinase,
showed PET degrading ability (Jabloune et al., 2020). Ideonella
sakaiensis produced two enzymes, PETase and MHETase (encoded by
ISF6_4831 and ISF6_0224), hydrolyzing PET efficiently into two
environmentally benign monomers, i.e., terephthalic acid (TPA) and
ethylene glycol (EG; Yoshida et al., 2016). PETase contained a
Ser-His-Asp catalytic triad at the active site, and its catalytic
mechanism was revealed (Joo et al., 2018). Then, PETase was found
have structural characteristics of lipase and cutinase, and a method
for degradation of high crystallinity PET catalyzed by this enzyme
was established (Austin et al., 2018). IsPETase variants with improved
thermal stability and much higher PET degradation activities were
developed (Son et al., 2020). In addition, a suberinase with remarkable
stability and capability to hydrolyse PET to terephthalic acid and
other polymers was sourced from Streptomyces scabies (Jabloune
et al., 2020). Furthermore, a dual enzyme system composed of
polyester hydrolase and carboxylesterase enhanced the biocatalytic
degradation of PET films (Barth et al., 2016). Moreover, 504 possible
PET hydrolase candidate genes from databases were identified, and
349 putative PET hydrolases were detected by analyzing 108 marine
and 25 terrestrial metagenomes. PET hydrolase genes were found
mainly in the phylum Bacteroidetes in marine metagenomes, and in
Actinobacteria and Proteobacteria in terrestrial metagenomes (Danso
et al., 2018). Four novel PET hydrolase genes were cloned, expressed
heterologously and their biochemical traits were described, moreover,
two displayed thermal stability and potential application value (Danso
et al., 2018).

Frontiers in Microbiology 09 frontiersin.org

Zhai et al.
FIGURE 3
The mechanism of microplastic biodegradation.
4. Plastisphere and quorum sensing
Quorum sensing (QS) refers to the cell-to-cell communication
process that is mediated by the production, release, accumulation and
group-wide detection of extracellular signaling molecules. These regulate
biological behaviors, such as bioluminescence, secondary metabolite
production and biofilm formation (Mukherjee and Bassler, 2019). Gram
negative bacteria mainly rely on N-acylhomoserine lactones (AHLs) as
their autoinducers (Williams et al., 2007), whereas Gram positive bacteria
mostly use autoinduced peptides (Schaefer et al., 2008).
QS plays an important role in the formation of bacterial biofilms.
QS will be induced when planktonic microorganisms proliferate to a
certain cell density on a medium, promoting more bacteria to attach,
leading to a mature biofilm (Costerton et al., 1995). It was demonstrated
that the stages of bacterial biofilm formation, attachment, maturation,
aggregation and dispersal, are always regulated by QS, which affects the
structure of biofilms (Parsek and Greenberg, 2005). For example, rhlI/R
and lasI/R are AHL-dependent QS systems in Pseudomonas aeruginosa.
Rhl system influences greatly the formation of biofilm (Mattmann et al.,
2008). The las system determines the structural differences of bacterial
biofilms, and exerts an important role in the irreversible adhesion phase
of the film-forming process (Lin et al., 2012). Studies on Burkholderia
cepacia (Brackman et al., 2009), Aeromonas hydrophila (Lynch et al.,
2002), Yersinia pseudotuberculosis (Atkinson et al., 1999), Vibrio
cholerae (Ye and Lu, 2010) and Staphylococcus (Kiran et al., 2008)
showed that QS could regulate bacterial aggregation and surface
adhesion. Furthermore, QS was found to play an important role in the
degradation of marine organic particles by Pantoea ananatis and
Ruegeria mobilis (Su et al., 2018). Also, quorum sensing is involved in
marine snow, and its possible influence on production of extracellular
hydrolytic enzymes in Pantoea ananatis B9 (Jatt et al., 2015).
Although the relevant research has not yet occurred, it is reasonable
to believe that QS has the potential to affect the formation and composition
of the plastisphere. Studies have showed that Rhodobacteraceae occupied
Frontiers in Microbiology
10.3389/fmicb.2023.1127308
core populations in the plastisphere (Debroas et al., 2017; Dussud et al.,
2018) and accounted for 16.4% in bacterial biofilms of MPs in the Yangtze
River Estuary, China (Jiang et al., 2018). A high proportion of
Rhodobacteraceae in the plastisphere was attributed to the conserved and
widespread QS signaling molecules participating in various metabolic
regulations, especially flagellum movement and biofilm formation on
plastic particles (Zan et al., 2014). QS may help Rhodobacteraceae attach
and aggregate on the surface of MPs, and inhibit other bacteria, including
Gammaproteobacteria. The primary model of QS regulation to the
plastisphere is shown in Figure 4. In addition, QS bacteria, which were
isolated from MPs, exhibited strong biofilm-forming ability and favorable
conditions for epiphytic growth. Thus, Oceanicola sp. strain D3 with QS
ability was isolated from a PVC biofilm (Li et al., 2019). Interestingly,
bacteriostasis, algae inhibition and the dimethylsulphoniopropionate
(DMSP) degradation function of QS bacteria may impact the pollution of
MPs in the marine environment (Gagné, 2017).
QS has the potential to be a new way to study marine MP biofilms
and their degradation. On the one hand, QS has a profound impact on
the microbial communities and the succession of biofilms, and the
bacteria may have an important role in regulating the process of
plastisphere formation. This may not only increase QS bacterial
colonization on MPs by producing extracellular polysaccharides, but
also inhibit the adhesion of other bacteria by producing antibacterial
materials. Conversely, QS regulates many metabolic functions of
dominant bacteria and enlarges their ecological function. For example,
AHLs may change the activity of extracellular hydrolases (Jatt et al.,
2015). Thus, a QS system based on AHLs may have a key role in the
degradation of MPs. Moreover, bacterial interaction based on the QS
network may provide a new perspective for the degradation of marine
MPs. The dominant colonization and rapid sensitivity to organic
substances may allow QS bacteria to be effective indicators for
monitoring MP pollution in the marine environment. Consequently,
understanding the plastisphere and promoting MPs degradation by QS
is expected to become a new research perspective.
10 frontiersin.org
Zhai et al.
FIGURE 4
The regulation of quorum sensing in the plastisphere.
5. Future directives
Plastic pollution is a problem that needs to be solved urgently, and
has gained growing public and scientific attention in recent years. In this
review, the formation process and microbial community composition of
plastisphere – the biofilm colonizing on plastic, the bacteria and the
enzymes as well as their degrading mechanism of MPs are discussed. In
particular, we clarified the potential role of QS in plastic research for the
first time. This may well offer novel ideas to the study of plastic
pollution control.
Microorganisms provide a new perspective for the exploration of
plastic treatment, however, research on the plastisphere still needs to
be advanced. The understanding of the distribution of MPs, the
microbial community structure and formation process of the
plastisphere and potential degrading bacteria of MPs need to be fully
explored. Future studies could be categorized mainly into three themes.
Firstly, more geographical distributions of MPs and biofilms and
comparisons of different materials, types of plastics and plastic area/
color are needed. These studies will help form the global distribution
pattern of MPs, and composition of biofilms (similarities and
differences), as well as promote regional targeted MP pollution control.
Studying the heterogeneity of microbial community structure in the
plastisphere and biofilms will lay the foundation for exploring the
metabolism and MPs degradation ability of bacteria. Secondly, more
investigations are needed on the effects of single bacterial strains and
communities on degradation. Methods of exploring the characteristics
of materials as the basal point, optimizing degradation conditions, using
bioinformatics to analyze the environmental response of relevant
metabolic genes in the habitat, as well as creating high-efficiency MP
degrading bacterial consortia should be undertaken. Thirdly, new
molecular techniques and in-situ characterization of isolated strains are
needed. Specific degradation pathways and degradation enzymes need
to be found to fully develop the known non-specific pathways to
metabolize plastics. In addition, the study of QS could focus on the
distribution, proportion and metabolism of QS bacteria in the
Frontiers in Microbiology
10.3389/fmicb.2023.1127308
plastisphere, which will help deepen the understanding of plastisphere
and potential degrading bacteria of MP.
Author contributions
MY and X-HZ: conceptualization. XZ: writing—original draft. XZ,
MY, and X-HZ: writing—review and editing. X-HZ: resources and
funding acquisition. All authors contributed to the article and approved
the submitted version.
Funding
This work was funded by the Scientific and Technological
Innovation Project of Laoshan Laboratory (nos. LSKJ202203200 and
2022QNLM030004-3), the National Natural Science Foundation of
China (nos. 41730530 and 92251303), and the Fundamental Research
Funds for the Central Universities (no. 202172002).
Conflict of interest
The authors declare that the research was conducted in the absence
of any commercial or financial relationships that could be construed as
a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and
do not necessarily represent those of their affiliated organizations, or
those of the publisher, the editors and the reviewers. Any product that
may be evaluated in this article, or claim that may be made by its
manufacturer, is not guaranteed or endorsed by the publisher.
11 frontiersin.org
Zhai et al.
References
Ahmad, M., Li, J.-L., Wang, P.-D., Hozzein, W. N., and Li, W.-J. (2020). Environmental
perspectives of microplastic pollution in the aquatic environment: a review. Mar. Life Sci.
Technol. 2, 414–430. doi: 10.1007/s42995-020-00056-w
Akdogan, Z., and Guven, B. (2019). Microplastics in the environment: a critical review
of current understanding and identification of future research needs. Environ. Pollut.
254:113011. doi: 10.1016/j.envpol.2019.113011
Amaral-Zettler, L. A., Zettler, E. R., and Mincer, T. J. (2020). Ecology of the plastisphere.
Nat. Rev. Microbiol. 18, 139–151. doi: 10.1038/s41579-019-0308-0
Amaral-Zettler, L. A., Zettler, E. R., Slikas, B., Boyd, G. D., Melvin, D. W., Morrall, C. E.,
et al. (2016). The biogeography of the Plastisphere: implications for policy. Front. Ecol.
Environ. 13, 541–546. doi: 10.1890/150017
Amin, S. A., Parker, M. S., and Armbrust, E. V. (2012). Interactions between diatoms and
bacteria. Microbiol. Mol. Biol. Rev. 76, 667–684. doi: 10.1128/MMBR.00007-12
Amobonye, A., Bhagwat, P., Singh, S., and Pillai, S. (2021). Plastic biodegradation:
frontline microbes and their enzymes. Sci. Total Environ. 759:143536. doi: 10.1016/j.
scitotenv.2020.143536
Antić, M. P., Jovancićević, B. S., Ilić, M., Vrvić, M. M., and Schwarzbauer, J. (2006).
Petroleum pollutant degradation by surface water microorganisms. Environ. Sci. Pollut.
Res. Int. 13, 320–327. doi: 10.1065/espr2006.03.296
Arias-Andres, M., Kettner, M. T., Miki, T., and Grossart, H. P. (2018). Microplastics:
new substrates for heterotrophic activity contribute to altering organic matter cycles
in aquatic ecosystems. Sci. Total Environ. 635, 1152–1159. doi: 10.1016/j.
scitotenv.2018.04.199
Asmita, K., Shubhamsingh, T., and Tejashree, S. (2015). Isolation of plastic degrading
micro-organisms from soil samples collected at various locations in Mumbai, India. Int. J.
Environ. Res. 4, 77–85.
Atkinson, S., Throup, J. P., Stewart, G. S., and Williams, P. (1999). A hierarchical quorum-
sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and
clumping. Mol. Microbiol. 33, 1267–1277. doi: 10.1046/j.1365-2958.1999.01578.x
Austin, H. P., Allen, M. D., Donohoe, B. S., Rorrer, N. A., Kearns, F. L., Silveira, R. L.,
et al. (2018). Characterization and engineering of a plastic-degrading aromatic polyesterase.
Proc. Natl. Acad. Sci. U. S. A. 115, E4350–e4357. doi: 10.1073/pnas.1718804115
Auta, H. S., Emenike, C. U., and Fauziah, S. H. (2017). Screening of bacillus strains
isolated from mangrove ecosystems in peninsular Malaysia for microplastic degradation.
Environ. Pollut. 231, 1552–1559. doi: 10.1016/j.envpol.2017.09.043
Auta, H. S., Emenike, C. U., Jayanthi, B., and Fauziah, S. H. (2018). Growth kinetics and
biodeterioration of polypropylene microplastics by bacillus sp. and Rhodococcus sp.
isolated from mangrove sediment. Mar. Pollut. Bull. 127, 15–21. doi: 10.1016/j.
marpolbul.2017.11.036
Balasubramanian, V., Natarajan, K., Hemambika, B., Ramesh, N., Sumathi, C. S.,
Kottaimuthu, R., et al. (2010). High-density polyethylene (HDPE)-degrading potential
bacteria from marine ecosystem of gulf of Mannar, India. Lett. Appl. Microbiol. 51,
205–211. doi: 10.1111/j.1472-765X.2010.02883.x
Barth, M., Honak, A., Oeser, T., Wei, R., Belisário-Ferrari, M. R., Then, J., et al. (2016).
A dual enzyme system composed of a polyester hydrolase and a carboxylesterase enhances
the biocatalytic degradation of polyethylene terephthalate films. Biotechnol. J. 11,
1082–1087. doi: 10.1002/biot.201600008
Bollinger, A., Thies, S., Knieps-Grünhagen, E., Gertzen, C., Kobus, S., Höppner, A., et al.
(2020). A novel polyester hydrolase from the marine bacterium pseudomonas aestusnigri—
structural and functional insights. Front. Microbiol. 11:114. doi: 10.3389/fmicb.2020.00114
Brackman, G., Hillaert, U., Van Calenbergh, S., Nelis, H. J., and Coenye, T. (2009). Use
of quorum sensing inhibitors to interfere with biofilm formation and development in
Burkholderia multivorans and Burkholderia cenocepacia. Res. Microbiol. 160, 144–151.
doi: 10.1016/j.resmic.2008.12.003
Bryant, J. A., Clemente, T. M., Viviani, D. A., Fong, A. A., Thomas, K. A., Kemp, P., et al.
(2016). Diversity and activity of communities inhabiting plastic debris in the North Pacific
Gyre. ASM J. 1, e00024–e00016. doi: 10.1128/mSystems.00024-16
Cappello, S., Caruso, G., Bergami, E., Macrì, A., Venuti, V., Majolino, D., et al.
(2021). New insights into the structure and function of the prokaryotic communities
colonizing plastic debris collected in King George Island (Antarctica): preliminary
observations from two plastic fragments. J. Hazard. Mater. 414:125586. doi: 10.1016/j.
jhazmat.2021.125586
Carozza, L., Berger, J. F., Burenscarozza, A., and Cyril, M. (2015). Microbial surface
colonization and biofilm development in marine environments. Microbiol. Mol. Biol. R
80:91. doi: 10.1128/MMBR.00037-15
Carson, H. S., Nerheim, M. S., Carroll, K. A., and Eriksen, M. (2013). The plastic-
associated microorganisms of the North Pacific gyre. Mar. Pollut. Bull. 75, 126–132. doi:
10.1016/j.marpolbul.2013.07.054
Chen, Z., Zhao, W., Xing, R., Xie, S., Yang, X., Cui, P., et al. (2020). Enhanced in situ
biodegradation of microplastics in sewage sludge using hyperthermophilic composting
technology. J. Hazard. Mater. 384:121271. doi: 10.1016/j.jhazmat.2019.121271
Cheng, J., Jacquin, J., Conan, P., Pujo-Pay, M., Barbe, V., George, M., et al. (2020).
Relative influence of plastic debris size and shape, chemical composition and
phytoplankton-bacteria interactions in driving seawater plastisphere abundance, diversity
and activity. Front. Microbiol. 11:610231. doi: 10.3389/fmicb.2020.610231
Frontiers in Microbiology
10.3389/fmicb.2023.1127308
Claessens, M., Clerck, K. D., Landuyt, L. V., Meester, S. D., and Janssen, C. R. (2011).
Occurrence and distribution of microplastics in marine sediments along the Belgian coast.
Mar. Pollut. Bull. 62, 2199–2204. doi: 10.1016/j.marpolbul.2011.06.030
Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., and Lappin-Scott, H. M.
(1995). Microbial biofilms. Annu. Rev. Microbiol. 49, 711–745. doi: 10.1146/annurev.
mi.49.100195.003431
Dang, H., Li, T., Chen, M., and Huang, G. (2008). Cross-ocean distribution of
Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters.
Appl. Environ. Microbiol. 74, 52–60. doi: 10.1128/AEM.01400-07
Danko, A. S., Luo, M., Bagwell, C. E., Brigmon, R. L., and Freedman, D. L. (2004).
Involvement of linear plasmids in aerobic biodegradation of vinyl chloride. Appl. Environ.
Microbiol. 70, 6092–6097. doi: 10.1128/AEM.70.10.6092-6097.2004
Danso, D., Schmeisser, C., Chow, J., Zimmermann, W., Wei, R., Leggewie, C., et al.
(2018). New insights into the function and global distribution of polyethylene terephthalate
(PET)-degrading bacteria and enzymes in marine and terrestrial metagenomes. Appl.
Environ. Microbiol. 84, e02773–e02717. doi: 10.1128/AEM.02773-17
Das, G., Bordoloi, N. K., Rai, S. K., Mukherjee, A. K., and Karak, N. (2012). Biodegradable
and biocompatible epoxidized vegetable oil modified thermostable poly(vinyl chloride):
thermal and performance characteristics post biodegradation with Pseudomonas
aeruginosa and Achromobacter sp. J. Hazard. Mater. 209-210, 434–442. doi: 10.1016/j.
jhazmat.2012.01.043
Davey, M. E., and O’Toole, G. A. (2003). Microbial biofilms: from ecology to molecular
genetics. Microbiol. Mol. Biol. Rev. 64, 847–867. doi: 10.1128/MMBR.64.4.847-867.2000
De Tender, C. A., Devriese, L. I., Haegeman, A., Maes, S., Ruttink, T., and Dawyndt, P.
(2015). Bacterial community profiling of plastic litter in the Belgian part of the North Sea.
Environ. Sci. Technol. 49, 9629–9638. doi: 10.1021/acs.est.5b01093
De Tender, C. A., Devriese, L. I., Haegeman, A., Maes, S., Vangeyte, J., Cattrijsse, A., et al.
(2017). Temporal dynamics of bacterial and fungal colonization on plastic debris in the
North Sea. Environ. Sci. Technol. 51, 7350–7360. doi: 10.1021/acs.est.7b00697
Debroas, D., Mone, A., and Ter Halle, A. (2017). Plastics in the North Atlantic garbage
patch: a boat-microbe for hitchhikers and plastic degraders. Sci. Total Environ. 599-600,
1222–1232. doi: 10.1016/j.scitotenv.2017.05.059
Deepika, S., and Madhuri, R. J. (2015). Biodegradation of low density polyethylene by
micro-organisms from garbage soil. J. Exp. Biol. Agric. Sci. 3, 15–21. doi: 10.1016/j.
jenvman.2020.110402
Delacuvellerie, A., Cyriaque, V., Gobert, S., Benali, S., and Wattiez, R. (2019). The
plastisphere in marine ecosystem hosts potential specific microbial degraders including
Alcanivorax borkumensis as a key player for the low-density polyethylene degradation. J.
Hazard. Mater. 380:120899. doi: 10.1016/j.jhazmat.2019.120899
Denaro, R., Aulenta, F., Crisafi, F., Di Pippo, F., Cruz Viggi, C., Matturroet, B., et al.
(2020). Marine hydrocarbon-degrading bacteria breakdown poly(ethylene terephthalate)
(PET). Sci. Total Environ. 749:141608. doi: 10.1016/j.scitotenv.2020.141608
Dussud, C., Meistertzheim, A. L., Conan, P., Pujo-Pay, M., George, M., Fabre, P., et al.
(2018). Evidence of niche partitioning among bacteria living on plastics, organic particles
and surrounding seawaters. Environ. Pollut. 236, 807–816. doi: 10.1016/j.
envpol.2017.12.027
Eriksen, M., Lebreton, L. C., Carson, H. S., Thiel, M., Moore, C. J., Borerro, J. C., et al.
(2014). Plastic pollution in the world's oceans: more than 5 trillion plastic pieces weighing
over 250,000 tons afloat at sea. PLoS One 9:e111913. doi: 10.1371/journal.pone.0111913
Erni-Cassola, G., Wright, R. J., Gibson, M. I., and Christie-Oleza, J. A. (2020). Early
colonization of weathered polyethylene by distinct bacteria in marine coastal seawater.
Microb. Ecol. 79, 517–526. doi: 10.1007/s00248-019-01424-5
Frère, L., Maignien, L., Chalopin, M., Huvet, A., Rinnert, E., Morrison, H., et al. (2018).
Microplastic bacterial communities in the bay of Brest: influence of polymer type and size.
Environ. Pollut. 242, 614–625. doi: 10.1016/j.envpol.2018.07.023
Gagné, F. (2017). Toxicity and disruption of quorum sensing in Aliivibrio fisheri by
environmental chemicals: impacts of selected contaminants and microplastics. J. Xenobiot.
7:7101. doi: 10.4081/xeno.2017.7101
Gajendiran, A., Krishnamoorthy, S., and Abraham, J. (2016). Microbial degradation of
low-density polyethylene (LDPE) by Aspergillus clavatus strain JASK1 isolated from
landfill soil. 3 Biotech 6:52. doi: 10.1007/s13205-016-0394-x
Gan, Z., and Zhang, H. (2019). PMBD: a comprehensive plastics microbial
biodegradation database. Database 2019:baz119. doi: 10.1093/database/baz119
Gao, R., and Sun, C. (2021). A marine bacterial community capable of degrading
poly(ethylene terephthalate) and polyethylene. J. Hazard. Mater. 416:125928. doi: 10.1016/j.
jhazmat.2021.125928
Giacomucci, L., Raddadi, N., Soccio, M., Lotti, N., and Fava, F. (2019). Polyvinyl chloride
biodegradation by pseudomonas citronellolis and Bacillus flexus. N. Biotechnol. 52, 35–41.
doi: 10.1016/j.nbt.2019.04.005
Giacomucci, L., Raddadi, N., Soccio, M., Lotti, N., and Fava, F. (2020). Biodegradation
of polyvinyl chloride plastic films by enriched anaerobic marine consortia. Mar. Environ.
Res. 158:104949. doi: 10.1016/j.marenvres.2020.104949
Gómez-Méndez, L. D., Moreno-Bayona, D. A., Poutou-Piñales, R. A., Salcedo-Reyes, J. C.,
Pedroza-Rodríguez, A. M., Vargas, A., et al. (2018). Biodeterioration of plasma pretreated
12 frontiersin.org
Zhai et al. 10.3389/fmicb.2023.1127308

LDPE sheets by Pleurotus ostreatus. PLoS One 13:e0203786. doi: 10.1371/journal. Kirstein, I. V., Wichels, A., Gullans, E., Krohne, G., and Gerdts, G. (2019). The
pone.0203786 Plastisphere—uncovering tightly attached plastic "specific" microorganisms. PLoS One
14:e0215859. doi: 10.1371/journal.pone.0215859
Gregory, M. R. (2009). Environmental implications of plastic debris in marine settings-
-entanglement, ingestion, smothering, hangers-on, hitch-hiking and alien invasions. Philos. Kong, F., Hong, K. J., Hang, X. U., Zhao, S. G., and Wang, Y. P. (2018). Evidence of
Trans. R. Soc. Lond. B Biol. Sci. 364, 2013–2025. doi: 10.1098/rstb.2008.0265 polystyrene biodegradation by gut microbiota of Styrofoam-feeding yellow
mealworms(larvae of Tenebrio molitor Linnaeus). Microbiol. China 45, 1438–1449.
Hadad, D., Geresh, S., and Sivan, A. (2005). Biodegradation of polyethylene by the
thermophilic bacterium Brevibacillus borstelensis. J. Appl. Microbiol. 98, 1093–1100. doi: Kowalczyk, A., Chyc, M., Ryszka, P., and Latowski, D. (2016). Achromobacter
10.1111/j.1365-2672.2005.02553.x xylosoxidans as a new microorganism strain colonizing high-density polyethylene as a key
step to its biodegradation. Environ. Sci. Pollut. Res. Int. 23, 11349–11356. doi: 10.1007/
Hall-Stoodley, L., Costerton, J. W., and Stoodley, P. (2004). Bacterial biofilms: from the
s11356-016-6563-y
natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95–108. doi: 10.1038/
nrmicro821 Krueger, M. C., Harms, H., and Schlosser, D. (2015). Prospects for microbiological
solutions to environmental pollution with plastics. Appl. Microbiol. Biotechnol. 99,
Hansen, J., Melchiorsen, J., Ciacotich, N., Gram, L., and Sonnenschein, E. C. (2021).
8857–8874. doi: 10.1007/s00253-015-6879-4
Effect of polymer type on the colonization of plastic pellets by marine bacteria. FEMS
Microbiol. Lett. 368:fnab026. doi: 10.1093/femsle/fnab026 Kumari, A., Chaudhary, D. R., and Jha, B. (2019). Destabilization of polyethylene and
polyvinylchloride structure by marine bacterial strain. Environ. Sci. Pollut. Res. Int. 26,
Harrison, J. P., Sapp, M., Schratzberger, M., and Osborn, A. M. (2011). Interactions
1507–1516. doi: 10.1007/s11356-018-3465-1
between microorganisms and marine microplastics: a call for research. Mar. Technol. Soc.
J. 45, 12–20. doi: 10.4031/MTSJ.45.2.2 Kyaw, B. M., Champakalakshmi, R., Sakharkar, M. K., Lim, C. S., and Sakharkar, K. R.
(2012). Biodegradation of low density polythene (LDPE) by pseudomonas species. Indian
Harshvardhan, K., and Jha, B. (2013). Biodegradation of low-density polyethylene by
J. Microbiol. 52, 411–419. doi: 10.1007/s12088-012-0250-6
marine bacteria from pelagic waters, Arabian Sea, India. Mar. Pollut. Bull. 77, 100–106. doi:
10.1016/j.marpolbul.2013.10.025 Lagarde, F., Olivier, O., Zanella, M., Daniel, P., Hiard, S., and Caruso, A. (2016).
Microplastic interactions with freshwater microalgae: hetero-aggregation and changes in
Harvey, B. P., Kerfahi, D., Jung, Y., Shin, J. H., Adams, J. M., and Hall-Spencer, J. M.
plastic density appear strongly dependent on polymer type. Environ. Pollut. 215, 331–339.
(2020). Ocean acidification alters bacterial communities on marine plastic debris. Mar.
doi: 10.1016/j.envpol.2016.05.006
Pollut. Bull. 161:111749. doi: 10.1016/j.marpolbul.2020.111749
Lambert, S., and Wagner, M. (2016). Formation of microscopic particles during the
Iiyoshi, Y., Tsutsumi, Y., and Nishida, T. (1998). Polyethylene degradation by lignin-
degradation of different polymers. Chemosphere 161, 510–517. doi: 10.1016/j.
degrading fungi and manganese peroxidase. J. Wood Sci. 44, 222–229. doi: 10.1007/
chemosphere.2016.07.042
BF00521967
Lee, O. O., Chung, H., Yang, J., Wang, Y., Dash, S., Wang, H., et al. (2014). Molecular
Ivar do Sul, J. A., Spengler, Â., and Costa, M. F. (2009). Here, there and everywhere. Small
techniques revealed highly diverse microbial communities in natural marine biofilms on
plastic fragments and pellets on beaches of Fernando de Noronha (equatorial Western
polystyrene dishes for invertebrate larval settlement. Microb. Ecol. 68, 81–93. doi: 10.1007/
Atlantic). Mar. Pollut. Bull. 58, 1236–1238. doi: 10.1016/j.marpolbul.2009.05.004
s00248-013-0348-3
Ivk, A., Aw, A., Gk, B., and Gg, A. (2018). Mature biofilm communities on synthetic
Lee, J. W., Nam, J. H., Kim, Y. H., Lee, K. H., and Lee, D. H. (2008). Bacterial communities
polymers in seawater—specific or general?—ScienceDirect. Mar. Environ. Res. 142,
in the initial stage of marine biofilm formation on artificial surfaces. J. Microbiol. 46,
147–154. doi: 10.1016/j.marenvres.2018.09.028
174–182. doi: 10.1007/s12275-008-0032-3
Jabloune, R., Khalil, M., Ben Moussa, I. E., Simao-Beaunoir, A. M., Lerat, S.,
Leys, N. M., Ryngaert, A., Bastiaens, L., Verstraete, W., Top, E. M., and Springael, D.
Brzezinski, R., et al. (2020). Enzymatic degradation of p-nitrophenyl esters, polyethylene
(2004). Occurrence and phylogenetic diversity of Sphingomonas strains in soils
terephthalate, cutin, and suberin by sub1, a suberinase encoded by the plant pathogen
contaminated with polycyclic aromatic hydrocarbons. Appl. Environ. Microbiol. 70,
Streptomyces scabies. Microbes Environ. 35:ME19086. doi: 10.1264/jsme2.ME19086
1944–1955. doi: 10.1128/AEM.70.4.1944-1955.2004
Jacquin, J., Cheng, J., Odobel, C., Pandin, C., Conan, P., Pujo-Pay, M., et al. (2019).
Li, Q., Xu, X., He, C., Zheng, L., Gao, W., Sun, C., et al. (2019). Complete genome
Microbial ecotoxicology of marine plastic debris: a review on colonization and
sequence of a quorum-sensing bacterium, Oceanicola sp. strain D3, isolated from a
biodegradation by the "Plastisphere". Front. Microbiol. 10:865. doi: 10.3389/
microplastic surface in coastal water of Qingdao, China. Microbiol. Resour. Announc. 8,
fmicb.2019.00865
e01022–e01019. doi: 10.1128/MRA.01022-19
Jambeck, J. R., Geyer, R., Wilcox, C., Siegler, T. R., Perryman, M., Andrady, A., et al.
Lin, L., Tan, X., and Jia, A. (2012). Relationship between bacterial quorum sensing and
(2015). Marine pollution. Plastic waste inputs from land into the ocean. Science 347,
biofilm formation--a review. Acta Microbiol. Sin. 52, 271–278.
768–771. doi: 10.1126/science.1260352
Liu, Y., Liu, W., Yang, X., Wang, J., Lin, H., and Yang, Y. (2021). Microplastics are a
Jang, M., Shim, W. J., Han, G. M., Song, Y. K., and Hong, S. H. (2018). Formation of
hotspot for antibiotic resistance genes: Progress and perspective. Sci. Total Environ.
microplastics by polychaetes (Marphysa sanguinea) inhabiting expanded polystyrene
773:145643. doi: 10.1016/j.scitotenv.2021.145643
marine debris. Mar. Pollut. Bull. 131, 365–369. doi: 10.1016/j.marpolbul.2018.04.017
Lynch, M. J., Swift, S., Kirke, D. F., Keevil, C. W., Dodd, C. E., and Williams, P. (2002).
Jatt, A. N., Tang, K., Liu, J., Zhang, Z., and Zhang, X. H. (2015). Quorum sensing in
The regulation of biofilm development by quorum sensing in Aeromonas hydrophila.
marine snow and its possible influence on production of extracellular hydrolytic enzymes
Environ. Microbiol. 4, 18–28. doi: 10.1046/j.1462-2920.2002.00264.x
in marine snow bacterium Pantoea ananatis B9. FEMS Microbiol. Ecol. 91, 1–13. doi:
10.1093/femsec/fiu030 Mattmann, M. E., Geske, G. D., Worzalla, G. A., Chandler, J. R., Sappington, K. J.,
Greenberg, E. P., et al. (2008). Synthetic ligands that activate and inhibit a quorum-sensing
Jeon, H. J., and Kim, M. N. (2015). Functional analysis of alkane hydroxylase system
regulator in Pseudomonas aeruginosa. Bioorg. Med. Chem. Lett. 18, 3072–3075. doi:
derived from Pseudomonas aeruginosa E7 for low molecular weight polyethylene
10.1016/j.bmcl.2007.11.095
biodegradation. Int. Bioderer Biodegr. 103, 141–146. doi: 10.1016/j.ibiod.2015.04.024
Mohan, A. J., Sekhar, V. C., Bhaskar, T., and Nampoothiri, K. M. (2016). Microbial
Jiang, P., Zhao, S., Zhu, L., and Li, D. (2018). Microplastic-associated bacterial
assisted high impact polystyrene (HIPS) degradation. Bioresour. Technol. 213, 204–207.
assemblages in the intertidal zone of the Yangtze estuary. Sci. Total Environ. 624, 48–54.
doi: 10.1016/j.biortech.2016.03.021
doi: 10.1016/j.scitotenv.2017.12.105
Mor, R., and Sivan, A. (2008). Biofilm formation and partial biodegradation of
Joo, S., Cho, I. J., Seo, H., Son, H. F., Sagong, H. Y., Shin, T. J., et al. (2018). Structural
polystyrene by the actinomycete Rhodococcus ruber: biodegradation of polystyrene.
insight into molecular mechanism of poly(ethylene terephthalate) degradation. Nat.
Biodegradation 19, 851–858. doi: 10.1007/s10532-008-9188-0
Commun. 9:382. doi: 10.1038/s41467-018-02881-1
Mukherjee, S., and Bassler, B. L. (2019). Bacterial quorum sensing in complex and
Kawai, F., Oda, M., Tamashiro, T., Waku, T., Tanaka, N., Yamamoto, M., et al. (2014). A
dynamically changing environments. Nat. Rev. Microbiol. 17, 371–382. doi: 10.1038/
novel Ca2+-activated, thermostabilized polyesterase capable of hydrolyzing polyethylene
s41579-019-0186-5
terephthalate from Saccharomonospora viridis AHK190. Appl. Microbiol. Biotechnol. 98,
10053–10064. doi: 10.1007/s00253-014-5860-y Nauendorf, A., Krause, S., Bigalke, N. K., Gorb, E. V., Gorb, S. N., Haeckel, M., et al.
(2016). Microbial colonization and degradation of polyethylene and biodegradable plastic
Kesy, K., Oberbeckmann, S., Kreikemeyer, B., and Labrenz, M. (2019). Spatial
bags in temperate fine-grained organic-rich marine sediments. Mar. Pollut. Bull. 103,
environmental heterogeneity determines young biofilm assemblages on microplastics in
168–178. doi: 10.1016/j.marpolbul.2015.12.024
Baltic Sea mesocosms. Front. Microbiol. 10:1665. doi: 10.3389/fmicb.2019.01665
Nowak, B., PająK, J., Drozd-Bratkowicz, M., and Rymarz, G. (2011). Microorganisms
Khan, S., Nadir, S., Shah, Z. U., Shah, A. A., Karunarathna, S. C., Xu, J., et al. (2017).
participating in the biodegradation of modified polyethylene films in different soils under
Biodegradation of polyester polyurethane by aspergillus tubingensis. Environ. Pollut. 225,
laboratory conditions. Int. Bioderer Biodegr. 65, 757–767. doi: 10.1016/j.ibiod.2011.04.007
469–480. doi: 10.1016/j.envpol.2017.03.012
Oberbeckmann, S., Kreikemeyer, B., and Labrenz, M. (2018). Environmental factors
Kiran, M. D., Adikesavan, N. V., Cirioni, O., Giacometti, A., Silvestri, C., Scalise, G., et al.
support the formation of specific bacterial assemblages on microplastics. Front. Microbiol.
(2008). Discovery of a quorum-sensing inhibitor of drug-resistant staphylococcal
8:2709. doi: 10.3389/fmicb.2017.02709
infections by structure-based virtual screening. Mol. Pharmacol. 73, 1578–1586. doi:
10.1124/mol.107.044164 Oberbeckmann, S. L. M., and Labrenz, M. (2015). Marine microplastic-associated
biofilms – a review. Environ. Chem. 12, 551–562. doi: 10.1071/EN15069
Kirstein, I. V., Kirmizi, S., Wichels, A., Garin-Fernandez, A., Erler, R., Löder, M., et al.
(2016). Dangerous hitchhikers? Evidence for potentially pathogenic vibrio spp. on Oberbeckmann, S., Loeder, M. G., Gerdts, G., and Osborn, A. M. (2014). Spatial and
microplastic particles. Mar. Environ. Res. 120, 1–8. doi: 10.1016/j.marenvres.2016.07.004 seasonal variation in diversity and structure of microbial biofilms on marine plastics in

Frontiers in Microbiology 13 frontiersin.org

Zhai et al.
northern European waters. FEMS Microbiol. Ecol. 90, 478–492. doi:
10.1111/1574-6941.12409
Oberbeckmann, S., Osborn, A. M., and Duhaime, M. B. (2016). Microbes on a bottle:
substrate, season and geography influence community composition of microbes colonizing
marine plastic debris. PLoS One 11:e0159289. doi: 10.1371/journal.pone.0159289
Ogonowski, M., Motiei, A., Ininbergs, K., Hell, E., Gerdes, Z., Udekwu, K. I., et al. (2018).
Evidence for selective bacterial community structuring on microplastics. Environ.
Microbiol. 20, 2796–2808. doi: 10.1111/1462-2920.14120
Oliveira, M. M., Proenca, A. M., Moreira-Silva, E., de Castro, A. M., Dos Santos, F. M.,
Marconatto, L., et al. (2021). Biofilms of pseudomonas and Lysinibacillus marine strains
on high-density polyethylene. Microb. Ecol. 81, 833–846. doi: 10.1007/s00248-020-01666-8
Onda, D. F. L., and Sharief, K. M. (2021). “Identification of Microorganisms Related to
Microplastics,” in Handbook of Microplastics in the Environment. eds. T. Rocha-Santos, M.
Costa and C. Mouneyrac (Cham: Springer).
Orr, I. G., Hadar, Y., and Sivan, A. (2004). Colonization, biofilm formation and
biodegradation of polyethylene by a strain of Rhodococcus ruber. Appl. Microbiol.
Biotechnol. 65, 97–104. doi: 10.1007/s00253-004-1584-8
Paço, A., Duarte, K., da Costa, J. P., Santos, P. S. M., Pereira, R., Pereira, M. E., et al.
(2017). Biodegradation of polyethylene microplastics by the marine fungus Zalerion
maritimum. Sci. Total Environ. 586, 10–15. doi: 10.1016/j.scitotenv.2017.02.017
Park, S. Y., and Kim, C. G. (2019). Biodegradation of micro-polyethylene particles by
bacterial colonization of a mixed microbial consortium isolated from a landfill site.
Chemosphere 222, 527–533. doi: 10.1016/j.chemosphere.2019.01.159
Parsek, M. R., and Greenberg, E. P. (2005). Sociomicrobiology: the connections between
quorum sensing and biofilms. Trends Microbiol. 13, 27–33. doi: 10.1016/j.tim.2004.11.007
Pathak, V. (2017). Review on the current status of polymer degradation: a microbial
approach. Bioresourc. Bioprocess. 4:15. doi: 10.1186/s40643-017-0145-9
Peeken, I., Primpke, S., Beyer, B., Gütermann, J., Katlein, C., Krumpen, T., et al. (2018).
Arctic Sea ice is an important temporal sink and means of transport for microplastic. Nat.
Commun. 9:1505. doi: 10.1038/s41467-018-03825-5
Peixoto, J., Silva, L. P., and Krüger, R. H. (2017). Brazilian Cerrado soil reveals an
untapped microbial potential for unpretreated polyethylene biodegradation. J. Hazard.
Mater. 324, 634–644. doi: 10.1016/j.jhazmat.2016.11.037
Peng, X., Chen, M., Chen, S., Dasgupta, S., and Bai, S. (2018). Microplastics contaminate
the deepest part of the world's ocean. Geochem. Perspect. Lett. 9, 1–5. doi: 10.7185/
geochemlet.1829
Pichel, W. G., Churnside, J. H., Veenstra, T. S., Foley, D. G., Friedman, K. S.,
Brainard, R. E., et al. (2007). Marine debris collects within the North Pacific subtropical
convergence zone. Mar. Pollut. Bull. 54, 1207–1211. doi: 10.1016/j.marpolbul.2007.04.010
Pinto, M., Langer, T. M., Hüffer, T., Hofmann, T., and Herndl, G. J. (2019). The
composition of bacterial communities associated with plastic biofilms differs between
different polymers and stages of biofilm succession. PLoS One 14:e0217165. doi: 10.1371/
journal.pone.0217165
Pollet, T., Berdjeb, L., Garnier, C., Durrieu, G., Le Poupon, C., Misson, B., et al. (2018).
Prokaryotic community successions and interactions in marine biofilms: the key role of
flavobacteriia. FEMS Microbiol. Ecol. 94:10.1093. doi: 10.1093/femsec/fiy083
Prata, J. C., Silva, A. L. P., Walker, T. R., Duarte, A. C., and Rocha-Santos, T. (2020).
COVID-19 pandemic repercussions on the use and management of plastics. Environ. Sci.
Technol. 54, 7760–7765. doi: 10.1021/acs.est.0c02178
Roager, L., and Sonnenschein, E. C. (2019). Bacterial candidates for colonization and
degradation of marine plastic debris. Environ. Sci. Technol. 53, 11636–11643. doi: 10.1021/
acs.est.9b02212
Rummel, C. D., Jahnke, A., Gorokhova, E., Kühnel, D., and Schmitt-Jansen, M. (2017).
Impacts of biofilm formation on the fate and potential effects of microplastic in the aquatic
environment. Environ. Sci. Technol. Lett. 4, 258–267. doi: 10.1021/acs.estlett.7b00164
Sangeetha Devi, R., Rajesh Kannan, V., Nivas, D., Kannan, K., Chandru, S., and Robert
Antony, A. (2015). Biodegradation of HDPE by aspergillus spp. from marine ecosystem of
gulf of Mannar. India. Mar. Pollut. Bull. 96, 32–40. doi: 10.1016/j.marpolbul.2015.05.050
Santo, M., Weitsman, R., and Sivan, A. (2013). The role of the copper-binding enzyme
– laccase – in the biodegradation of polyethylene by the actinomycete Rhodococcus ruber.
Int. Bioderer Biodegr. 84, 204–210. doi: 10.1016/j.ibiod.2012.03.001
Schaefer, A. L., Greenberg, E. P., Oliver, C. M., Oda, Y., Huang, J. J., Bittan-Banin, G.,
et al. (2008). A new class of homoserine lactone quorum-sensing signals. Nature 454,
595–599. doi: 10.1038/nature07088
Shah, A. A., Hasan, F., Hameed, A., and Ahmed, S. (2008). Biological degradation of
plastics: a comprehensive review. Biotechnol. Adv. 26, 246–265. doi: 10.1016/j.
biotechadv.2007.12.005
Shen, M., Zhu, Y., Zhang, Y., Zeng, G., Wen, X., Yi, H., et al. (2019). Micro(nano)plastics:
Unignorable vectors for organisms. Mar. Pollut. Bull. 139, 328–331. doi: 10.1016/j.
marpolbul.2019.01.004
Singh, L., and Wahid, Z. A. (2015). Methods for enhancing bio-hydrogen production
from biological process: a review. J. Ind. Eng. Chem. 21, 70–80. doi: 10.1016/j.
jiec.2014.05.035
Son, H. F., Joo, S., Seo, H., Sagong, H. Y., Lee, S. H., Hong, H., et al. (2020). Structural
bioinformatics-based protein engineering of thermo-stable PETase from Ideonella
sakaiensis. Enzyme Microb. Technol. 141:109656. doi: 10.1016/j.enzmictec.2020.109656
Frontiers in Microbiology
10.3389/fmicb.2023.1127308
Su, Y., Tang, K., Liu, J., Wang, Y., Zheng, Y., and Zhang, X. (2018). Quorum sensing
system of Ruegeria mobilis Rm01 controls lipase and biofilm formation. Front. Microbiol.
9:3304. doi: 10.3389/fmicb.2018.03304
Sucato, A., Vecchioni, L., Savoca, D., Presentato, A., Arculeo, M., and Alduina, R.
(2021). A comparative analysis of quatic and Ppolyethylene-associated antibiotic-
resistant bicrobiota in the Mediterranean Sea. Biology 10:200. doi: 10.3390/
biology10030200
Sudhakar, M., Trishul, A., Doble, M., Kumar, K. S., Jahan, S. S., Inbakandan, D., et al.
(2007). Biofouling and biodegradation of polyolefins in ocean waters. Polym. Degrad. Stab.
92, 1743–1752. doi: 10.1016/j.polymdegradstab.2007.03.029
Sun, X., Chen, B., Xia, B., Li, Q., Zhu, L., Zhao, X., et al. (2020). Impact of mariculture-
derived microplastics on bacterial biofilm formation and their potential threat to
mariculture: a case in situ study on the Sungo Bay, China. Environ. Pollut. 262:114336. doi:
10.1016/j.envpol.2020.114336
Syranidou, E., Karkanorachaki, K., Amorotti, F., Avgeropoulos, A., Kolvenbach, B.,
Zhou, N. Y., et al. (2019). Biodegradation of mixture of plastic films by tailored marine
consortia. J. Hazard. Mater. 375, 33–42. doi: 10.1016/j.jhazmat.2019.04.078
Tahir, L., Ishtiaq Ali, M., Zia, M., Atiq, N., Hasan, F., and Ahmed, S. (2013). Production
and characterization of esterase in Lantinus tigrinus for degradation of polystyrene. Pol. J.
Microbiol. 62, 101–108. doi: 10.33073/pjm-2013-015
Tischler, D., Eulberg, D., Lakner, S., Kaschabek, S. R., van Berkel, W. J., and
Schlömann, M. (2009). Identification of a novel self-sufficient styrene monooxygenase
from Rhodococcus opacus 1CP. J. Bacteriol. 191, 4996–5009. doi: 10.1128/JB.00307-09
Tribedi, P., and Sil, A. K. (2014). Cell surface hydrophobicity: a key component in the
degradation of polyethylene succinate by pseudomonas sp. AKS2. J. Appl. Microbiol. 116,
295–303. doi: 10.1111/jam.12375
Urbanek, A. K., Rymowicz, W., and Mirończuk, A. M. (2018). Degradation of plastics
and plastic-degrading bacteria in cold marine habitats. Appl. Microbiol. Biotechnol. 102,
7669–7678. doi: 10.1007/s00253-018-9195-y
Van Cauwenberghe, L., Claessens, M., Vandegehuchte, M. B., Mees, J., and Janssen, C. R.
(2013). Assessment of marine debris on the Belgian continental shelf. Mar. Pollut. Bull. 73,
161–169. doi: 10.1016/j.marpolbul.2013.05.026
Wang, Z., An, C., Chen, X., Lee, K., Zhang, B., and Feng, Q. (2021). Disposable masks
release microplastics to the aqueous environment with exacerbation by natural weathering.
J. Hazard. Mater. 417:126036. doi: 10.1016/j.jhazmat.2021.126036
Wilkes, R. A., and Aristilde, L. (2017). Degradation and metabolism of synthetic plastics
and associated products by pseudomonas sp.: capabilities and challenges. J. Appl. Microbiol.
123, 582–593. doi: 10.1111/jam.13472
Williams, P., Winzer, K., Chan, W. C., and Cámara, M. (2007). Look who's talking:
communication and quorum sensing in the bacterial world. Philos. Trans. R. Soc. Lond. B
Biol. Sci. 362, 1119–1134. doi: 10.1098/rstb.2007.2039
Woodall, L. C., Jungblut, A. D., Hopkins, K., Hall, A., Robinson, L. F., Gwinnett, C.,
et al. (2018). Deep-sea anthropogenic macrodebris harbours rich and diverse
communities of bacteria and archaea. PLoS One 13:e0206220. doi: 10.1371/journal.
pone.0206220
Wright, R. J., Erni-Cassola, G., Zadjelovic, V., Latva, M., and Christie-Oleza, J. A. (2020).
Marine plastic debris: a new surface for microbial colonization. Environ. Sci. Technol. 54,
11657–11672. doi: 10.1021/acs.est.0c02305
Wright, R. J., Langille, M. G. I., and Walker, T. R. (2021). Food or just a free ride? A
meta-analysis reveals the global diversity of the Plastisphere. ISME J. 15, 789–806. doi:
10.1038/s41396-020-00814-9
Xie, H., Chen, J., Feng, L., He, L., Zhou, C., Hong, P., et al. (2021). Chemotaxis-selective
colonization of mangrove rhizosphere microbes on nine different microplastics. Sci. Total
Environ. 752:142223. doi: 10.1016/j.scitotenv.2020.142223
Xu, X., Wang, S., Gao, F., Li, J., Zheng, L., Sun, C., et al. (2019). Marine microplastic-
associated bacterial community succession in response to geography, exposure time, and
plastic type in China's coastal seawaters. Mar. Pollut. Bull. 145, 278–286. doi: 10.1016/j.
marpolbul.2019.05.036
Yang, Y., Liu, W., Zhang, Z., Grossart, H. P., and Gadd, G. M. (2020). Microplastics
provide new microbial niches in aquatic environments. Appl. Microbiol. Biotechnol. 104,
6501–6511. doi: 10.1007/s00253-020-10704-x
Yang, J., Yang, Y., Wu, W. M., Zhao, J., and Jiang, L. (2014). Evidence of polyethylene
biodegradation by bacterial strains from the guts of plastic-eating waxworms. Environ. Sci.
Technol. 48, 13776–13784. doi: 10.1021/es504038a
Yang, Y., Yang, J., Wu, W., Zhao, J., Song, Y., Gao, L., et al. (2015a). Biodegradation and
mineralization of polystyrene by plastic-eating mealworms: part 1. Chemical and physical
characterization and isotopic tests. Environ. Sci. Technol. 49, 12080–12086. doi: 10.1021/
acs.est.5b02661
Yang, Y., Yang, J., Wu, W., Zhao, J., Song, Y., Gao, L., et al. (2015b). Biodegradation
and mineralization of polystyrene by plastic-eating mealworms: part 2. Role of gut
microorganisms. Environ. Sci. Technol. 49, 12087–12093. doi: 10.1021/acs.
est.5b02663
Ye, X., and Lu, C. (2010). Advance in quorum-sensing system to affect vibrio cholerae
biofilm formation. J. Microbiol. 30, 80–83.
Yoon, M. G., Jeon, H. J., and Kim, N. M. (2012). Biodegradation of polyethylene by a soil
bacterium and alkb cloned recombinant cell. J. Bioremed. Biodegr. 3:145. doi:
10.4172/2155-6199.1000145
14 frontiersin.org
Zhai et al. 10.3389/fmicb.2023.1127308

Yoshida, S., Hiraga, K., Takehana, T., Taniguchi, I., Yamaji, H., Maeda, Y., et al. (2016). moth galleria mellonella. Sci. Total Environ. 704:135931. doi: 10.1016/j.
A bacterium that degrades and assimilates poly(ethylene terephthalate). Science 351, scitotenv.2019.135931
1196–1199. doi: 10.1126/science.aad6359
Zhang, X., Li, Y., Ouyang, D., Lei, J., Tan, Q., Xie, L., et al. (2021a). Systematical review
Yuan, J., Ma, J., Sun, Y., Zhou, T., Zhao, Y., and Yu, F. (2020). Microbial degradation and of interactions between microplastics and microorganisms in the soil environment. J.
other environmental aspects of microplastics/plastics. Sci. Total Environ. 715:136968. doi: Hazard. Mater. 418:126288. doi: 10.1016/j.jhazmat.2021.126288
10.1016/j.scitotenv.2020.136968
Zhang, K., Shi, H., Peng, J., Wang, Y., Xiong, X., Wu, C., et al. (2018). Microplastic
Zan, J., Liu, Y., Fuqua, C., and Hill, R. T. (2014). Acyl-homoserine lactone quorum pollution in China's inland water systems: a review of findings, methods, characteristics,
sensing in the Roseobacter clade. Int. J. Mol. Sci. 15, 654–669. doi: 10.3390/ijms15010654 effects, and management. Sci. Total Environ. 630, 1641–1653. doi: 10.1016/j.
Zettler, E. R., Mincer, T. J., and Amaral-Zettler, L. A. (2013). Life in the "plastisphere": scitotenv.2018.02.300
microbial communities on plastic marine debris. Environ. Sci. Technol. 47, 7137–7146. doi:
Zhang, X., Zhang, Y., Wu, N., Li, W., Song, X., Ma, Y., et al. (2021b). Colonization
10.1021/es401288x
characteristics of bacterial communities on plastic debris: the localization of
Zhang, J., Gao, D., Li, Q., Zhao, Y., Li, L., Lin, H., et al. (2020). Biodegradation of immigrant bacterial communities. Water Res. 193:116883. doi: 10.1016/j.
polyethylene microplastic particles by the fungus aspergillus flavus from the guts of wax watres.2021.116883

Frontiers in Microbiology 15 frontiersin.org